Pakistan J. Zool., vol. 47(2), pp. 545-550, 2015.

Biodiversity of Species, Interactions with Horticultural Crops and a New Record for

Gulay Kacar Plant Protection Department, Agriculture and Natural Science Faculty, Abant Izzet Baysal University, Golkoy, Bolu, 14280, Turkey

Abstract.- are an important predator group across many terrestrial crop systems. A survey was conducted in 2009 to determine the compositoin and abundance of spider species in citrus, persimmon, carob, avocado, almond, loquat, fig, and pomegranate plants in the eastern Mediterranean region of Turkey. Spiders were collected by using a beating method with steiner funnel and a hand aspirator. In total, 45 spider species were identified from 21 families. The taxonomic families of Gnaphosidae, Miturgidae, Salticidae, Theridiidae and Thomosidae were commonly sorted. Twenty-nine species belonging to 16 families were found on citrus trees. Adult/juvenile rate observed was 42%, and male/female rate was 48%, with most juveniles being female. Spider biodiversity was determined using the Shannon-Wiener diversity index according to spider distribution on each crop plant. Although each crop sheltered certain spider species, no avocado-specific spiders were found. The biodiversity index was the highest for Diponema sp. and Chericanthium sp.. Among the colllected species was Clubiona juvenis (Simon, 1878) (Clubionidae), found on the loquat trees, and representing a new record for this spider species in Turkey.

Key words: Clubiona juvenis, biodiversity, horticultural crops, spider, Shannon-Wiener index.

INTRODUCTION fauna in Turkey have been less commonly made in there is little information about spider fauna in some of Turkey’s more important agricultural areas. Spiders are an important group with regard Surveys in agriculture that were conducted include to species diversity, ranking seventh in global studies in sainfoin fields of Van province in the east, diversity after insect orders (Mahalakshmi and grapes of Aegean region, almond orchards of Jeyaparvathi, 2014). Spiders can be found in nearly eastern and southeastern Anatolia regions, cereal all habitats, surviving under a wide range of fields of Antalya province and alfalfa fields of ecological conditions. Therefore, spiders can be a Mardin and Şanlıurfa provinces (Bayram et al., good indicator taxon to reflect ecological change. 1999; Goven et al., 2002; Danısman et al., 2007; Spiders also have a role in ecosystem services, and Bolu et al., 2008; Efil et al., 2012). Researchers are one of the main predators in many have rarely studied in the horticultural crops, the habitats (Cardosa et al., 2011). spider species in the eastern Mediterranean region, Spiders include over 114 families, in nearly however, with the notable exception of Ozturk et al. 4,000 genera and around 45,000 species in the world (2013) who reported 59 spiders belonging to 17 (Platnick, 2014). Spider fauna have been studied in families in pomegranate and olive orchards in a different habitats in Turkey (Ayhan, 2004; Demir, small (regional) area that including 16 locations. 2004; Soysal, 2004; Yenigun, 2006; Seyyar, 2009; This study aimed to determine spider species Demir et al., 2010; Yalcın 2010; Akpınar, 2011; composition and abundances, as well as Kunt et al., 2011; Bayram et al., 2014). According characteristics of families found on different fruit to recent studies, the checklist of the spider species trees in the eastern Mediterranean region. Because in Turkey includes over 930 species belonging to 42 of the Mediterranean climate, which is relatively families (Bayram et al., 2014). However, surveys of stable and includes very warm summers and mild spider agricultural systems and, as a result, winters, most cultivated plants are fruit trees (especially citrus, olive, grapes, pomegranate, ______persimmon, almond, and others) and field plants * Corresponding author: [email protected] (corn, cotton, vegatables, wheat, watermelon, and 0030-9923/2015/0002-0545 $ 8.00/0 others). Surveys were conducted in persimmon, Copyright 2015 Zoological Society of 546 G. KACAR almond, avocado, carob, citrus, fig, loquat, and orchards. Persimmon can be found within the pomegranate plants in 2009. The spider species sampled region in home gardens or fully grown composition on different fruit trees was compared plants in the orchards. by a biodiversity analysis in terms of their family and species compositions. Collecting and identifying spiders Spider collections were taken monthly, from MATERIALS AND METHODS March to September in 2009. At each site, trees were sampled at random and on each tree branches Sample sites were sampled from the four cardinal directions The sampled sites were in agricultural areas (north, east, south and west). The collected samples near Adana, Hatay, and Mersin provinces in the were sorted from trees according to Lazarov and eastern Mediterranean region of Turkey (Fig. 1). Grigorov (1961) (Table I). For each sample, spiders The site locations range from near the coast of the were collected by shaking and knocking the branch Mediterranean Sea (Cukurova basin- Adana, Mersin three times over a 1 m² section of tree foliage and and Amik basin- Hatay) to mountainous regions that the dislodged spiders would drop into a funnel have an altitude near 1000 meters. In total, an area shaped collector and then were collected with a of nearly 35.500 km2 was represented by the hand aspirator and placed into glass jars. The sampled sites, ranging from 33-37º north collected samples were brought to the laboratory of hemisphere meridians and 36-38º north hemisphere Adana Biological Research Control Station where parallels. The sampled regions represent typical the spiders were killed, put into 70% alcohol, Mediterranean climates: hot dry summers and wet labeled and then sent to taxonomic expert for mild winters, with the mountainous areas slightly identification. We pooled 199 total samples from cooler than the coastal areas sampled. eight crops in 49 different orchards.

Table I.- The number of samples collected varied according to Sample plants the number of trees available for sampling, based on Spider species were sampled from eight sampling progression described by Lazarov and cultivated plants: almond, avocado, carob, citrus, Grigorov (1961) persimmon, fig, loquat, and pomegranate. Citrus is Total trees in orchard Number of trees sampled the one of the main crops in the eastern Mediterranean region and is grown primarily in the 1-20 All trees 21-70 10–30 flat basin regions where there is irrigation available. 71-150 31–40 Oranges, mandarins, lemons, and grapefruits are the 151-500 41–80 501-1000 All trees %15 main citrus varieties. Lemons are cultivated in More than 1000 All trees %5 Mersin province, while mandarins and oranges are grown in Adana and Hatays. Because of the intensity of agricultural production, chemicals are Data analysis used to control pests in citrus orchards in the The Shannon-Wiener (S-W) diversity index Cukurova and Amik basins. Loquat is also grown, (H) was used to determine the biodiversity of the but there are only a few loquat orchards in the spider species for each horticultural plant. H is sampled regions. Pomegranate orchards have been calculated as H= - Pi(lnPi). Pi is the proportion of increasing in acreage in recent years and can be the each spider species every plant. Lnpi is the found separately at the edge of the other orchards natural log, PilnPi, a part of whole species and (especially citrus). Avocado and alligator pears are natural log of Pi, is found multiplying with Pi and commonly found as individual or small clusters of Lnpi. The value range of using the natural log is trees in the home gardens, with larger commercial from 0 to ~4.6, where 0 shows that every species in orchards more difficult to find. Fig, almond, and the sample is the same species in the same species carob are also commonly found as individual or and 4.6 is evenly distributed. Larger value reports small clusters of trees, often at the edge of the other that species found on many plant species and in BIODIVERSITY OF SPIDER SPECIES OF TURKEY 547 different places of the sampling areas. values were found in Dipoena sp. (-0.33), Chericanthium sp. (-0.21), Xysticus sp. (-0.17), RESULTS Theridion sp. (-0.14), Cheiracanthium mildei (- 0.13), Enoplognatha sp. (-0.12), Micaria sp. (-0.12), A total 45 spider species from 21 families Clubiona caerulescens (-0.10), Clubiona sp. (-0.09), were found in all horticultural orchards in this study. Dictyna lateens (-0.08), Linyphia tenuipalpis (- The common families were determined as 0.08). The greatest diversity in terms of samples Gnaphosidae, Miturgidae, Salticidae, Theridiidae (e.g., crop systems) was found in Diponema. and Thomosidae. The most common families Although spider species were found on many of the recorded were Salticidae and Therididae. On citrus, difference sampled crops, Ebrechtella sp., 29 species belonging to16 families were recovered. Macaroeris sp., Mimetus sp., Anyphaena On loquat, 15 species belonging to 10 families were accentuate, Aulonia albimana, Diplocephalus found, with the most commonly represented family picinus, Gibbaranea gibbosa, Harpactea sp., the Salticidae (4 species). On carob, 13 species, 13 Heliophanus auratus, Micaria dives, Neon sp., genera and 11 families were recorded, with the most Plexippoides gestroi, Prodidomus sp., Scotophaeus abundant family being the Therididae (3 species). scutulatus, Thomisus onustus, Trochosa sp. and From the other crops, we collected 12 species, 12 Zelotes gracilis had the lowest H values. The new genera, and 7 families, primarily from the species C. juvenis was found as -0.06 on the loquat Theridiidae (4 species) and Thomosidae (3 species). (Fig. 2). Across all surveyed crops, 45 different spider species were recorded, from the 244 spider individuals from 172 sampling areas, 92 individuals from 22 citrus orchards, 66 individuals from 8 loquat areas, 43 individuals from 9 carob areas and 43 individuals from other orchards areas (Table II). The new species record for Turkey of Clubiona juvenis was collected in loquat. Adult/juvenile rate observed was 42%, and male/female rate was 48%, with most juveniles being female. The male: female ratio was found as 35% in the citrus orchards, 23% in the loquat trees, 43% in the carob trees and 50% in the other sampled Fig. 1. Juvenile, male and female and rate of Araneae in different horticultural plants in crops, indicating that female were more commonly the eastern Mediterranean region of Turkey. collected than males in the major crop systems surveyed. Among identified species, the most variation of spider stages was determined in loquat and the lowest was found in fig trees. There was also a difference in the development stage and gender based on the crop system surveyed, with most juveniles found in pomegranates, most males found in avocado, and most females found in loquat, respectively (Fig. 1). There was also a difference in where different spider families were found; for example Clubionidae were most common in citrus and loquat trees. The Shannon-Wiener diversity index showed spider species were generally well distributed Fig. 2. Frequency of spider stages per plant in different horticultural plants in the among the all samples (H=3.35). Larger PilnPi eastern Mediterranean region of Turkey. 548 G. KACAR

Table II.- Spider species in the citrus plants in the eastern Mediterranean region of Turkey

Family name Species name Citrus Carob Loquat Pome- Parsi- Fig Almond Avakado granate mon

Agelenidae Tegenaria sp. 4 Tegenaria domestica (Clerck, 1757) 3 Amaurobiidae Amaurobius sp. 2 Anyphaena accentuata (Walckenaer, 1 1802) Anyphaenidae Anyphaena accentuata (Walckenaer, 1 1802) Araneidae Araneus sp. 1 Gibbaranea gibbosa (Walckenaer, 1802) 1 Gibbaranea sp. 3 Clubionidae Clubiona sp. 2 4 Clubiona caerulescens L. Koch, 1867 7 Clubiona juvenis Simon, 1878 * 3 Dictynidae Dictyna latens (Fabricius, 1775) 3 2 Dysderidae Harpactea sp. 1 Filistatidae Pritha sp. 2 Gnaphosidae Micaria sp. 2 2 2 3 Micaria dives (Lucas, 1846) 1 Scotophaeus scutulatus (L. Koch, 1866) 1 Zelotes gracilis (Canestrini, 1868) 1 Hahniidae Hahnia ononidum Simon, 1875 2 Linyphiidae Bolyphantes sp. 3 Diplocephalus picinus (Blackwall, 1841) 1 Linyphia tenuipalpis (Simon, 1884) 5 Lycosidae Trochosa sp. 1 Aulonia albimana (Walckenaer, 1805) 1 Mimetidae Mimetus sp. 1 Miturgidae Cheiracanthium mildei L. Koch, 1864 10 Chericanthium sp. 5 3 10 2 1 Pisauridae Pisaura mirabilis (Clerck, 1757) Philodromidae Philodromus sp. 3 2 Thanatus sp. 2 2 Philodromus margaritatus (Clerck, 1757) 4 Prodidomidae Prodidomus sp. 1 Salticidae Evarcha michailovi 3 Macaroeris sp. 1 Platnickia sp. 4 Heliophanus auratus C.L.Koch, 1835 1 Sitticus sp. 1 2 Ballus sp. 4 Salticus sp. 2 Salticus zebraneus (C.L.Koch, 1837) 2 Plexippoides gestroi (Dalmas, 1920) 1 Neon sp. 1 Thyene imperalis (Rossi, 1846) 3 Tinaoecidae Nurscia sp. 2 Theridiidae Dipoena sp. 20 11 18 2 4 Enoplognatha sp. 2 4 3 Euryopis flavomaculata (C.L.Koch,1836) 2 Robertus arunduneti (O.P.-Cambridge, 3 3 1871) Theridion sp. 4 4 3 Thomisidae Ebrechtella sp. 1 Thomisus sp. 2 Thomisus onustus Walckenaer, 1805 1 Xysticus sp. 2 6 3 4 Zodariidae Zodarion cyprium Kulczynski, 1908 3

Total 92 43 66 10 9 4 9 11

* new record for Turkey fauna BIODIVERSITY OF SPIDER SPECIES OF TURKEY 549

DISCUSSION Knowledge of spider species composition and distribution in other fruits is very limited from Our results provide one of the first Turkey and nearby regions. Ghavami (2008) descriptions of spider species in agricultural crops reported that 1231 specimens were classified in 45 systems in eastern Mediterranean region of Turkey. species and 36 genera belonged to 17 families from One of our more exciting finds was the new record pomegranate in (the families Lycosidae, for C. juvenis in Turkey. Previously, only ten Linyphiidae, Gnaphosidae and Theridiidae were Clubiona species have been recorded in Turkey most common). Mansoure et al. (1985) studied the (Bayram et al., 2014), and the addition of C. juvenis spider fauna on avocado foliage in and bring the total number of Clubionidae species to reported that Theridion spp. represented 63% and eleven in Turkey. The Clubiona ( Clubiona Clubiona 20% of all spiders collected. Latreille, 1804) is not a large group, with only 19 There have been other surveys of spider fauna species represented in . Spider species in this in some Turkish crop systems. Bolu et al. (2008) genus typically have a dull brownish or reddish gray reported that 129 specimens were collected in abdomen, are between 5-12 mm long, and hunt at Turkish almond orchards studied in the eastern night and spend the day in a cell of silk that can be (Elazıg) and southeastern Anatolia (Diyarbakır and found under stones and bark (Nieuwenhuys, 2015). Mardin provinces) regions, representing 21 species To put this into context with other Clubionidae, the belonging to 16 genera and 9 families (Agelenidae family contains 577 species in 15 genera in the Araneidae, Dictyniidae, Gnaphosidae, Linyphiidae, world (Platnick, 2014). Clubionids have been Philodromidae, Salticidae, Theridiidae, recorded previously in citrus, but were numerically Thomisidae). Because there have been relatively abundant; for example, Clubiona leucaspis has been few surveys of spider fauna in Turkey’s crop commonly found on citrus in a number of countries systems, there are still many new records yet to be (Benfatto and Franco, 1995) and Clubiona reichlini found. For example, Anyphaena sabina L. Koch, was the dominant species from citrus in (Zhi, 1866 (Anyphaenidae) is a new species from İzmir 2002a, 2002b). and Antalya orchards for Turkish spider fauna Because citrus is a key crop in this region of (Guven et al., 2008). In this study, 502 specimens Turkey, some comparisons between our survey were captured in pitfall traps and 284 specimens results and spiders found on citrus in other parts of collected using an aspirator; a total of 63 species the work is warranted. For example, spiders were determined (belong to 16 families) and of only representing 89 species that belonged to 17 families 63 species there was one new record for Turkey. were collected on citrus in ; the common The most encountered families recorded by Guven families were Theridiidae (18 species), Thomisidae et al. (2008) were Gnaphosidae, Lycosidae and (13 species), Araneidae (13 species) and Salticidae Thomisidae; the most captured species was Xysticus (10 species) (Benfatto and Franco, 1995). robusta (Hahn). In two other relatively recent Additionally, on citrus in , , a surveys, Gnaphosa opaca Hermann, Gnaphosa survey found spiders belonging to 20 families, 77 microps Holm, Zelotes aurantiacus Miller and genera and 140 species (Green, 1999). Twenty-eight Cicurina cicur (Fabricius) were recorded in Turkey species of spiders, belonging to 22 genera and 12 for the first time by Bayram et al. (1999) and ten families, were found in citrus orchards in China new species were record from citrus orchards of (Zhi, 2002a) and 34 spider species, 32 genera and Antalya by Teksam et al. (2010). 13 families were reported in Iran with the Araneidae The findings from our research and the other and Salticidae being the most common families recent surveys of spider fauna in Turkey indicate (Ghavami and Ghanadamooz, 2008). Finally, on that there is still much to be done and with greater citrus in Valencia, , collected spiders efforts more new records and new species will be represented 19 families (53 species) with Salticidae found in Turkey’s agricultural crops. For example, comprising 36.7% and Theridiidae with 27.7% of only seven Clubionid species were previously the collected spiders (Barrientos et al., 2010). reported from Turkey and it is believed and 550 G. KACAR expected that more species will be added to the list GHAVAMI, S. AND GHANADAMOOZ, S., 2008. 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